Revista Mexicana de Biodiversidad 83: 1036-1044, 2012

DOI: 10.7550/rmb.28124

Stem and root anatomy of two species of Echinopsis (Trichocereeae: Cactaceae)

Anatomía de la raíz y del tallo de dos especies de Echinopsis (Trichocereeae: Cactaceae)

Joelma dos Santos Garcia1, Edna Scremin-Dias1 and Patricia Soffiatti2

1
Universidade Federal de Mato Grosso do Sul, CCBS, Departamento de Biologia, Programa de Pós Graduação em Biologia Vegetal Cidade
Universitária, S/N, Caixa Postal 549, CEP 79.070.900 Campo Grande, MS, Brasil.
2
Universidade Federal do Paraná, SCB, Departamento de Botânica, Programa de Pós-Graduação em Botânica, Caixa Postal 19031, CEP 81.531.990
Curitiba, PR, Brasil.
psoffiatti.ufpr@gmail.com

Abstract. This study characterizes and compares the stem and root anatomy of Echinopsis calochlora and E. rhodotricha
(Cactaceae) occurring in the Central-Western Region of Brazil, in Mato Grosso do Sul State. Three individuals of each
species were collected, fixed, stored and prepared following usual anatomy techniques, for subsequent observation in
light and scanning electronic microscopy. Echinopsis calochlora revealed uniseriated epidermis, while E. rhodotricha
had patches of bisseriated epidermis; all species showed thick cuticle, parallelocytic stomata at the epidermis level, and
a well-developed hypodermis. Cortical and medullary bundles are present in the studied species, as well as mucilage
cells in the cortex region. The secondary phloem is composed by sieve tube elements, companion cells, axial and
radial parenchyma. Sclereids were found at the outer regions of phloem in the roots. The secondary xylem is non
fibrous in the stems of E. calochlora, and fibrous in the stems of E. rhodotricha and in the roots of both species. Many
of these characteristics are commonly found in Cactaceae, and represent important adaptations for survival in xeric
environments.

Key words: cortical bundles, epidermis, non fibrous wood, wood anatomy.

Resumen. Este estudio está enfocado a caracterizar y comparar la anatomía de tallos y raíces de Echinopsis calochlora
y E. rhodotricha (Cactaceae) que habitan en la región centro-oeste de Brasil, en el Estado de Mato Grosso do Sul.
Se recolectaron 3 individuos de cada especie, los cuales fueron fijados, almacenados y preparados siguiendo las
técnicas comunes de anatomía, para observarlos en microscopía de luz y electrónica de barrido. Echinopsis calochlora
mostró epidermis uniseriada, mientras que la de E. rhodotricha fue biseriada; todas las especies presentaron cutícula
gruesa, estomas paralelocíticos a nivel de la epidermis y una hipodermis bien desarrollada. Se presentaron haces
vasculares corticales y medulares en las especies estudiadas, así como células mucilaginosas en la región cortical. El
floema secundario está compuesto de elementos de tubo criboso, células acompañantes y parénquima axial y radial.
Se encontraron esclereidas en las regiones externas del floema en las raíces. El xilema secundario es no-fibroso en
los tallos de E. calochlora y fibroso en los de E. rhodotricha y en las raíces de ambas especies. Muchas de estas
características están presentes comúnmente en especies de Cactaceae, lo que representa adaptaciones importantes para
la supervivencia en ambientes xéricos.

Palabras clave: haces corticales, epidermis, madera no-fibrosa, anatomía de la madera.

Introduction Gibson and Nobel, 1986; Soffiatti and Angyalossy, 2003,

The subfamily Cactoideae (Cactaceae) comprises
the largest number of species, is the most diversified in
terms of life-forms and habit (Taylor, 2000; Terrazas
and Arias, 2003), and it is divided in 9 tribes, in which
Cereeae, Rhipsalideae, Trichocereeae, Echinocereeae, and
Hylocereeae occur in Brazil (Taylor and Zappi, 2004).
The importance of anatomical studies in Cactaceae
are undeniable (Gibson and Horak, 1978; Gasson, 1981;
Recibido: 20 octubre 2011; aceptado: 02 junio 2012
2005, 2007; Terrazas and Arias, 2003; Arruda et al., 2005),
considering the representativeness of the family, and the
problems in circumscribing groups, especially within
tribes, as well as enabling a better understanding of the
group evolution (Terrazas and Arias, 2003) and their
adaptations for survival in arid environments (Mauseth,
2006).
Eggli (2002) mentioned the lack of information on
Cactaceae in Brazil in the Brazilian southwestern region,
elaborating a checklist of 33 native species for the states
of Mato Grosso and Mato Grosso do Sul. From those, 27
Revista Mexicana de Biodiversidad 83: 1036-1044, 2012
DOI: 10.7550/rmb.28124
species belong to Cactoideae, and 6 genera were recorded
for tribe Trichocereeae: Arthrocereus (A. Berger) Backeb.
et F.M. Knuth, Cleistocactus Lem., Discocactus Pfeiff.,
Echinopsis Zucc., Gymnocalycium Pfeiffer in Pfeiffer et
Otto, and Harrisia Britton, all being very poorly studied,
especially in the state of Mato Grosso do Sul.
Echinopsis is one of the largest genus of Trichocereeae,
composed by 128 species distributed in several regions of
South America, and due to the large number of species,
it shows a very controversial circumscription (Anderson,
2001). Echinopsis calochlora K. Schum. is endemic to the
high altitudes of the Maciço do Urucum (Eggli, 2002), in
western Mato Grosso do Sul, and was recently included
in the Brazilian list of threatened species (IBAMA, 2008),
because its habitat has been intensively exploited, for iron
and manganese mining (Silva et al., 2000). Echinopsis
rhodotricha K. Schum. has a broader distribution,
occurring Brazil, Paraguay and Argentina (Anderson,
2001). This work describes comparatively the anatomy of
stem and root of E. calochlora and E. rhodotricha.
Materials and methods
Individuals were collected in rocky outcrops and
sandy-clay formations from natural populations as
follows: E. calochlora at Corumbá County, in Pantanal
(voucher number CGMS 17536; J. S. Garcia 54), and E.
rhodotricha, at Porto Murtinho, in Chaco (voucher number
CGMS 17590; J. S. Garcia 61). Vouchers were deposited
at the Herbarium - CGMS/UFMS, Federal University of
Mato Grosso do Sul.
For the qualitative anatomical study of the stem, 3
individuals of each species were sectioned at the basal,
medium, and apical regions. For the root, only the very base
was used. Samples were fixed with FAA 70 for 72 hours,
rinsed in water and stored in ethanol 70% (Jensen, 1962).
Paradermal sections were taken at the median region of the
stem. Transverse and longitudinal sections of stems and
roots were made by hand. Samples were also embedded
in polyethylene glycol (PEG) 1500 (Richter, 1985) and
transverse and longitudinal sections were made in rotative
microtome. Root samples of E. rhodotricha were sectioned
in a sliding microtome. Sections were stained with astrablue
and safranin and mounted in glycerine 50%. Macerations
were prepared using a modified Franklin method (Franklin,
1945), stained with safranin and mounted in glycerin.
The following hystochemical tests were carried out:
floroglucyn (Johansen, 1940) to detect lignified secondary
walls; lugol (Johansen, 1940) to detect starch; for mucilage
we followed Richter (1977). The analysis was carried out
in a Leica DMLB light microscope, connected to an image
capture system, and a digital camera DC 300F.
1037
Paradermal and transversal sections of the dermal
system of the stem median region were prepared for
scanning electron microscopy (SEM) analysis. Samples
were dehydrated, critical-point dried, mounted on aluminum
stubs, and coated with gold-palladium in a sputter system.
SEM analysis and electron micrographs were made with a
JEOL JSM 5800 scanning electron microscope.
Results
Stem. Uniseriate epidermis (Fig. 1) occurred in
photosynthesizing regions of the stem, as well as in
apical and median regions. It was composed by square
to rectangular cells in cross sections, with thick cuticle.
Echinopsis rhodotricha showed patches of bisseriate
epidermis in the median region (Fig. 2), formed by
periclinal divisions of epidermal cells, rarely observed in
E. calochlora.
Parallelocytic stomata were found in both species at
the same level of epidermal cells in E. calochlora (Fig.
1) while E. rhodotricha had sunken stomata (Fig. 2).
Substomatal chambers crossed the hypodermis (Figs. 1, 2).
The phellogen was originated in the epidermis.
Peridermis covered the non photosynthesizing portions
of the stem (Figs. 3, 4); composed of pheloderm formed
by rectangular cells in cross section, with primary walls.
Cork had layers of cells with suberized walls that alternate
with layers of cells with lignified walls, which are very
numerous in E. rhodotricha (Fig. 4).
We observed a collenchymatic hypodermis in the stem
(Figs. 1, 2, 5), composed of cells with irregularly thickened
primary walls, connecting through ramified channels.
Cortex was divided in an outer region forming a
palisade (Fig. 5), and an inner region composed of large
parenchyma cells and vascular bundles (Fig. 5), constituted
by phloem and xylem, arranged collaterally. Druses
were rare in the cortex. Large mucilage cells occurred
throughout the whole cortex (Fig. 6) and pith. Vascular
bundles occurred also in the pith (Fig. 7).
At the base of stem, primary phloem was collapsed
and in E. rhodotricha caps of sclereids were seen outside
secondary phloem (Fig. 8). Secondary phloem was
composed of narrow sieve tube elements and companion
cells, with simple sieve plate, transverse to slight oblique,
axial and radial parenchyma.
Both species had non fibrous wood, mainly composed
of wide band tracheids and a few vessel elements,
surrounded by axial and radial unlignified parenchyma
cells (Figs. 9-11). Wide band tracheids presented ring,
helical or mixed wall thickenings (Fig. 11). Vessel
elements had simple perforation plates. Both species had
a storied structure in the non fibrous wood (Fig. 11), being
1038 Garcia et al.- Anatomy of two species of Echinopsis

Figures 1-6. Stem cross sections. 1-2, epidermis covered by a thick cuticle (arrow). Stomata chamber crossed hypodermis. 1,
Echinopsis calochlora. Uniseriate epidermis. Stomata at the same level as ordinary epidermal cells. 2, E. rhodotricha. Scanning electron
micrograph (SEM). Bisseriate epidermis and sunken stomata. 3-4, peridermis with pheloderm composed of layers of parenchyma cells;
cork composed of layers of cells with suberized walls alternating with layers of cells with lignified walls (*). 3, E. calochlora. 4-6,
E. rhodotricha. 5, organization of cortex: hypodermis followed by layers of palisade parenchyma and inner isodiametric parenchyma
cells. Cortical bundles (arrows). 6, cortex. Numerous scattered mucilage cells. Scale bars: 1= 100 µm; 2= 5 µm; 3-4= 200 µm; 5= 500
µm; 6= 250 µm. Cm- mucilage cell; Ep- epidermis; Hp- hypodermis; Pp- palisade parenchyma; St- stomata; Su- suber.
Revista Mexicana de Biodiversidad 83: 1036-1044, 2012
DOI: 10.7550/rmb.28124 1039

Figures 7-12. 7-10, 12, cross sections. 11, tangential section. 7, Echinopsis calochlora. Pith with medullary bundle. 8, E. rhodotricha.
Vascular system. Phloem. Caps of sclereids in the periphery of secondary phloem. 9, E. calochlora. Non fibrous wood mainly composed
of wide band tracheids. 10, E. rhodotricha. Fibrous and non fibrous wood. 11, E. calochlora. Non fibrous wood composed of wide
band tracheids with helical thickenings. 12, E. rhodotricha. Fibrous wood composed of vessel elements, fibres and scanty paratracheal
parenchyma (part of a ray is seen on the left). Scale bars: 7, 9-12= 200 µm; 8= 400 µm. FW- fibrous wood; NFW- non fibrous wood.
1040
most pronounced in E. calochlora. Fibrous wood occurred
only in E. rhodotricha, outside non fibrous wood (Figs.10,
12-15), diffuse porous, with wide band tracheids absent,
composed of vessels predominantly solitary and multiples
of 2 to 3, and less frequent, of 4 to 5; vessel elements walls
had helical to pitted secondary walls; intervessel pits were
bordered; vessel-parenchyma pits simple to half-bordered,
scalariform, opposite to alternate; perforation plates were
simple (Fig. 14), transverse to oblique; some vessels had 3
perforation plates; intermediate forms between scalariform
with one incomplete bar to irregular and reticulate were
observed (Fig. 15). Parenchyma was scanty paratracheal
(Fig. 12). Multiseriate wide and high heterogeneous rays
(Fig. 13) were composed of procumbent, upright or/and
square cells, with lignified and unlignified portions; starch
grains occurred in ray cells (Figs. 10, 12). Libriform
fibres were present, rare septate. Bands of unlignified
parenchyma including axial and radial parenchyma were
present in fibrous wood (Fig. 10).
Root. Adult roots were covered by a peridermis, similar to
the stem (Fig. 16); composed of pheloderm formed by 5 to
6 layers of rectangular cells in cross section, with primary
walls; cork was formed by several layers of cells with
suberized walls, which alternate with layers of cells with
lignified walls.
Cortex was composed of parenchyma cells with
primary walls. Druses were less frequent in E. calochlora,
and absent in E. rhodotricha .
The primary phloem was collapsed (Figs. 16, 17),
with caps of sclereids outside secondary phloem (Fig.
17). Secondary phloem (Fig. 17) comprised narrow
and short sieve tube elements, with simple sieve plate,
transversal to slightly oblique; companion cells; axial
and radial parenchyma. Secondary xylem was fibrous in
both species (Figs. 16-20), diffuse porous, composed of
vessels predominantly solitary and multiples of 2 to 3,
and less frequent, of 4 to 5 vessel elements with simple
perforation plate, transverse to oblique; in E. rhodotricha,
intermediate forms between scalariform with one
incomplete bar to irregular and reticulate were observed,
similar to the stem fibrous wood; intervessel pits were
bordered; vessel-parenchyma pits were simple to half-
bordered, scalariform, opposite to alternate. Wide band
tracheids were absent. Scanty paratracheal parenchyma
present (Fig. 17). Unlignified, multiseriate wide and
high heterogeneous rays (Figs. 16-19) were composed
of procumbent, upright or/and square cells. Druses and
starch grains (Fig. 19) occurred in ray cells. Libriform
fibres were present, septate (rare) only in E. rhodotricha
(Fig. 20). Unlignified parenchyma was present including
also axial parenchyma, forming bands, more evident in
E. rhodotricha.
Garcia et al.- Anatomy of two species of Echinopsis
Discussion
The anatomical characteristics observed in the studied
species are commonly observed in other Cactaceae species,
as extensively described in the literature (Terrazas-Salgado
and Mauseth, 2002; Soffiatti and Angyalossy, 2003, 2007,
2009; Terrazas and Arias, 2003; Arruda et al., 2005;
Mauseth, 2006).
The 2 Echinopsis species have a thick cuticle, an
important adaptation for xeric habitats, protecting the
plant body from water loss and pathogens. Unusual in
Cactaceae (Gibson and Nobel, 1986; Loza-Cornejo and
Terrazas, 2003), they showed a secondarily biseriated
epidermis, which has also been reported for a few other
genera in Trichocereeae, such as Harrisia (Mauseth et
al., 1998); a multiseriate epidermis was mentioned for
Espostoa Britton and Rose (Mauseth, 1999). Reports
of multiseriated epidermis exist for other tribes such
as Pachycereeae (Gibson and Horak, 1978; Barthlott
and Hunt, 1993; Terrazas-Salgado and Mauseth,
2002), Cacteae (Terrazas-Salgado and Mauseth, 2002),
Notocacteae (Nyffeler and Eggli, 1997; Terrazas-Salgado
and Mauseth, 2002), Cereeae (Darling, 1989; Mauseth,
1996), and Browningieae (Mauseth, 1996). As stated by
Loza-Cornejo and Terrazas (2003), multiple epidermis in
cacti occur in unrelated genera and seem to have appeared
several times in Cactaceae.
Parallelocytic stomata and a long substomatal chamber
were observed in the investigated species, a common
feature for the members of the family (Gasson, 1981; Eggli,
1984). In contrast with most xerophytes, several species of
Cactaceae show superficial stomata (Eggli, 1984; Gibson
and Horak, 1978; Fahn and Cutler, 1992; Loza-Conejo and
Terrazas, 2003; Soffiatti and Angyalossy, 2007), where
guard cells are on the same level as the other epidermal
cells. The long substomatal chamber, due to the thick
hypodermis, reduces water loss when the stomata are open
(Fahn and Cutler, 1992). According to Darling (1989), the
reduced transpiration rates are combined with low CO2
and O2 exchange rates, prioritizing water conservation.
Sunken stomata were observed in E. rhodotricha, a
situation reported for some other genera (Metcalfe and
Chalk, 1950; Gasson, 1981; Eggli, 1984; Loza-Cornejo
and Terrazas, 2003), maximizing water loss prevention.
Nevertheless, this is a variable feature in the genus, once
superficial stomata were observed in other species, such as
in Echinopsis aurea Britton et Rose (Eggli, 1984), and in
E. calochlora, while in E. eyriesii (Turpin) Zucc. these are
sunken, as in E. rhodotricha.
The organization of cortical tissues in both studied
Echinopsis species is typical of cacti (Gibson and Nobel,
1986; Loza-Cornejo and Terrazas, 2003; Mauseth,
Revista Mexicana de Biodiversidad 83: 1036-1044, 2012
DOI: 10.7550/rmb.28124 1041

Figures 13-20. 13-15, stem secondary xylem; tangential sections. Echinopsis rhodotricha. 13, large rays. 14, simple perforation plate
of a vessel element. 15, incomplete perforation plate of a vessel element. 16-20, root and cross sections (16-19). 20, tangential section.
16-17, E. calochlora. 16, general view; note peridermis composed of several layers of cells with lignified walls alternate with cells
with suberized walls; fibrous wood with large unlignified rays. 17, phloem and xylem. Collapsed phloem (arrows) outside functional
secondary phloem. 18-19, E. rhodotricha. 18, fibrous wood with large unlignified rays. 19, detail of unlignified rays containing starch
grains. 20, E. calochlora tangential sections; septate fibres (arrows). Scale bars: 13= 400 µm; 14-15= 10 µm; 16, 18= 500 µm; 17= 100
µm; 19-20= 200 µm. Co-cortex; P- peridermis; Ph- phloem; R- rays; Xy- xylem
1042
2006; Soffiatti and Angyalossy, 2007): there is a thick
hypodermis composed of several layers of colenchymatic
cells, followed by a photosynthetic palisade parenchyma
and the inner cortex, composed of isodiametric
parenchymatic cells. The hypodermis, being a flexible
tissue, has important functions in giving support to the
stem and accommodating the stem changes in volume due
to shrinkage and swelling, also protecting the inner tissues
against pathogens (Gibson and Nobel, 1986). As the stems
in most cacti are the main photosynthesizing organ, the
organization of the chlorenchyma or palisade parenchyma
is very similar to a leaf (Sajeva and Mauseth, 1991). The
internal cortex cells store water (Mauseth, 1993b), and the
large cells are able to expand and contract depending on
hydration state or water availability (Mauseth, 2006).
Both species presented cortical and medullary bundles
with secondary growth, spread out in all directions very
similar to leaf veins. Like leaf veins, they are collateral
and form a network that extends to the base of the
palisade parenchyma. Cortical bundles are considered a
synapomorphy for Cactoideae, present in nearly all species
(Mauseth, 2006). They perform important functions
in sugar and water transport to and from cortex cells
and to the vascular system (Mauseth and Sajeva, 1992;
Terrazas-Salgado and Mauseth, 2002; Mauseth, 2006).
Mauseth (2004) considers that the presence of cortical
bundles explains the large volume of cortex, as succulent
euphorbias, for instance, do not possess cortical bundles
and their stems never reach such a large size as cacti.
Medullary bundles have the same function as cortical
bundles, transporting water and nutrients (Mauseth, 1993a,
2006; Terrazas-Salgado and Mauseth, 2002), occurring
only in Cactoideae (Mauseth, 1993a, 2006). According to
Gibson and Nobel (1986) pith diameter increased during
Cactaceae evolution and this event probably led to the
emergence of medullary bundles.
In the basal and older regions of the stem, as well as
in the root of these 2 Echinopsis species, the epidermis
is substituted by a peridermis, as noted for many species
in the family. The origin of phellogen from periclinal
divisions of epidermal cells is very common in cacti
(Gibson and Nobel, 1986; Terrazas-Salgado and Mauseth,
2002; Soffiatti and Angyalossy, 2003; Mauseth, 2006).
Although the origin of phellogen in a plant organ can be
variable, from different cell types, such as epidermal,
colenchymatic, parenchymatic or even phloematic cells,
the most common origin is from subepidermal layers
of cells, according to Evert (2006). It was seen in E.
calochlora and E. rhodotricha that phellem in both root
and stem is composed by layers of suberized cells which
alternate with layers of lignified cells, also a common
feature for species of the family (Mauseth, 2006).
Garcia et al.- Anatomy of two species of Echinopsis
The phloem was composed of sieve tube elements
and companion cells, axial and radial parenchyma and
sometimes, non functional phloem might become lignified,
similar to what was described for several Cactaceae stems
(Mauseth, 1999; Terrazas-Salgado and Mauseth, 2002;
Soffiatti and Angyalossy, 2003, Arruda et al., 2005;
Mauseth, 2006), and roots (Mauseth and Ross, 1988;
Mauseth, 1989). Echinopsis rhodotricha has fibre caps
outside phloem; in E. calochlora they are absent, typical
of species which have non fibrous wood (Mauseth et al.,
1998).
Echinopsis calochlora and E. rhodotricha present
fibrous wood in the roots while in the stems they both
have non fibrous wood, corroborating the fact established
by Mauseth and Stone-Palmquist (2001). These authors
stated that the structure of wood in the stem and root of the
same plant can be very different. Echinopsis rhodotricha
has also fibrous wood in the stem, characterizing what is
termed dimorphic wood: when young the plant produces
one type of wood and later on, the cambium produces
another type (Mauseth and Plemons, 1995; Mauseth and
Plemons-Rodríguez, 1998). In the present work, it was
observed a typical situation in E. rhodotricha: which first
forms non fibrous wood, when the body is young and
small and does not need special investment in support,
and when mature, the cambium starts forming fibrous
wood since support is then needed due to the larger size
(Terrazas-Salgado and Mauseth, 2002). The fibrous and
non fibrous wood types observed in the present study have
the same structure as described in literature, with fibrous
wood composed of vessel elements in a matrix of libriform
fibres, and non fibrous wood composed of vessel elements
in a matrix of wide band tracheids (Gibson, 1973; Gibson
and Nobel, 1986; Terrazas-Salgado and Mauseth, 2002;
Mauseth, 2006; Soffiatti and Angyalossy, 2009). The only
difference between the fibrous wood of the stem and root
of E. rhodotricha is the presence of the storied structure in
the stem, absent in the root. A noticeable feature observed
in the secondary xylem of the stem in both species is the
occurrence of a storied structure in the secondary xylem.
This feature has been described in the literature for several
species of Cactoideae, including E. calochlora, by Gibson
(1973). This author observed that the rays are rarely storied,
and mentions that the storied structure is more evident in
specialized growth forms, such as globose and epiphytic
species. Gibson (1973) also stated that in non fibrous wood
it is a difficult feature to distinguish due to differences in
the length of vessel elements and wide band tracheids, but
this was not the case in the present study. Storied wood is
a feature that occurs in several phylogenetically unrelated
groups and it is found in groups where fusiform cambial
initials are shorter (Carlquist, 2001). In the present study,
Revista Mexicana de Biodiversidad 83: 1036-1044, 2012
DOI: 10.7550/rmb.28124
the non fibrous wood showed a storied structure, especially
regarding wide band tracheids, more pronounced in E.
calochlora than E. rhodotricha.
Many of the characteristics presented in this work
corroborate the descriptions that had already been reported
for other species of Cactoideae. Some anatomical features
can be used as diagnostic, allowing for the segregation of
the 2 species of Echinopsis studied, such as: presence of
biseriated epidermis, sunken stomata, and fibrous and non
fibrous wood in the stem of E. rhodotricha. As Echinopsis
comprises a large number of species (ca. 128 species,
Anderson, 2001), some intrageneric variability is expected
for this genus, and more species should be investigated,
in order to establish the diagnostic value of those traits
mentioned.
Acknowledgements
Thanks to the “Fundação de Apoio ao Desenvolvimento
do Ensino, Ciência e Tecnologia do Estado de Mato Grosso
do Sul” (FUNDECT), for the master scholarship to the
first author, to the Research Coordinator – Pro-Reitoria de
Pesquisa e Pós-Graduação da Universidade Federal Mato
Grosso do Sul, from the Programa de Pós Graduação em
Biologia Vegetal, and the National Council of Research
(CNPq), process n. 473673/2007-0. We would like to thank
the Scanning Electronic Microscope Center of the Federal
University of Paraná, especially to the Dr. Cleusa Bona
due to the equipment use; to Dr. Geraldo Alves Damasceno
Jr. and the Msc. Vali Joana Pott for identifying the species
and to the “Pantanal Seeds Net” by the logistic support on
the field sampling.
Literature cited
Anderson, E. F. 2001. The cactus family. Timber Press, Portland,
Oxford. 776 p.
Arruda, E., G. F. Melo-De-Pinna and M. Alves. 2005.
Anatomia dos órgãos vegetativos de Cactaceae da caatinga
pernambucana. Revista Brasileira de Botânica 28:589-601.
Barthlott, W. and D. R. Hunt. 1993. Cactaceae. In The families
and genera of vascular plants, K. Kubitzki (ed.). Springer-
Verlag, Berlin. p. 161-197.
Carlquist, S. 2001. Comparative wood anatomy. Systematic,
ecological, and evolutionary aspects of dicotyledon wood,
2nd edition. Springer-Verlag, Berlin. 448 p.
Darling, M. S. 1989. Epidermis and hypodermis of the saguaro
cactus (Cereus giganteus): anatomy and spectral properties.
American Journal of Botany. 76:1698-1706.
Eggli, U. 1984. Stomatal types of Cactaceae. Plant Systematics
and Evolution 146:197-214.
Eggli, U. 2002. Synopsis of the Cactaceae of Mato Grosso,
1043
Brazil. Haseltonia 9:146-166.
Evert, R. F. 2006. Esau´s plant anatomy. Meristems, cells and
tissues of the plant body – Their structure, function and
development. 3rd edition, John Wiley & Sons, Inc., New
Jersey. 601 p.
Fahn, A. and D. F. Cutler. 1992. Xerophytes. Gebruder
Borntraeger. Berlin, Sttutgart. 178 p.
Franklin, G. L. 1945. Preparation of thin sections of synthetic
resins and wood-resin composites, and a new macerating
method for wood. Nature 155:51.
Gasson, P. 1981. Epidermal anatomy of some North American
globular cacti. The Cactus and Succulent Journal of Great
Britain 43:101-108.
Gibson, A. C. 1973. Comparative anatomy of secundary xylem
in Cactoideae (Cactaceae). Biotropica 5:29-65.
Gibson, A. C. and K. Horak. 1978. Systematic anatomy and
phylogeny of Mexican columnar cacti. Annals of the
Missouri Botanical Garden 65:1013-1057.
Gibson, A. C. and P. S. Nobel. 1986. The cactus primer. Harvard
University Press, Cambridge, London. 286 p.
IBAMA. 2008. Instrução Normativa nº 06, de 23 de setembro
de 2008. 55 p.
Jensen, W. A. 1962. Botanical histochemistry, principles and
practice. W. H. Freeman, San Francisco. p. 408.
Johansen, D. A. 1940. Plant microtechique. Mc Graw Hill
Book, New York. 523 p.
Loza-Cornejo, S. and T. Terrazas. 2003. Epidermal and
hypodermal characteristics in North American Cactoideae
(Cactaceae). Journal of Plant Research 116:27-35.
Mauseth, J. D. 1989. Comparative structure-function studies
within a strongly dimorphic plant, Melocactus intortus
(Cactaceae). Bradleya 7:1-12.
Mauseth, J. D. 1993a. Medullary bundles and the evolution of
cacti. American Journal of Botany 80:928-932.
Mauseth, J. D. 1993b. Water-storing and cavitation-preventing
adaptations in wood of cacti. Annals of Botany 72:81-89.
Mauseth, J. D. 1996. Comparative anatomy of tribes Cereeae
and Browningieae (Cactaceae). Bradleya 14:66-81.
Mauseth, J. D. 1999. Comparative anatomy of Espostoa,
Pseudoespostoa, Thrixanthocereus and Vatricania
(Cactaceae). Bradleya 17:27-37.
Mauseth, J. D. 2004. The structure of photosynthetic, succulent
stems in plants other than cacti. International Journal of
Plant Sciences 165:1-9.
Mauseth, J. D. 2006. Structure-function relationships in highly
modified shoots of Cactaceae. Annals of Botany 98:901-
926.
Mauseth, J. D. and B. J. Plemons. 1995. Developmentally
variable, polymorphic woods in cacti. American Journal of
Botany 82:1199-1205.
Mauseth, J. D. and B. J. Plemons-Rodriguez. 1998. Evolution
of extreme xeromorphic characters in wood: a study of
1044
nine evolutionary lines in Cactaceae. American Journal of
Botany 85:209-218.
Mauseth, J. D. and R. G. Ross. 1988. Systematic anatomy of
the primitive cereoid cactus Leptocereus quadricostatus.
Bradleya 6:49-64.
Mauseth, J. D. and M. Sajeva. 1992. Cortical bundles in the
persistent, photosynthetic stems of cacti. Annals of Botany
70:317-324.
Mauseth, J. D. and M. E. Stone-Palmquist. 2001. Root wood
differs strongly from shoot wood within individual plants
of many Cactaceae. International Journal of Plant Sciences
162:767-776.
Mauseth, J. D., T. Terrazas and S. Loza-Cornejo. 1998. Anatomy
of relictual members of Subfamily Cactoideae, IOS Group
1a (Cactaceae). Bradleya 16:31-43.
Metcalfe, C. R. and L. Chalk. 1950. Anatomy of Dicotyledons –
leaves, stem, and wood in relation to taxonomy with notes
on economic uses, volume I. Clarendon Press, Oxford. p.
724.
Nyffeler, R. and U. Eggli. 1997. Comparative stem anatomy and
systematics of Eriosyce sensu lato (Cactaceae). Annals of
Botany 80:767-786.
Richter, H. G. 1977. Differential staining of oil and mucilage in
idioblasts of Lauraceae. IAWA 4:76.
Richter, H. G. 1985. Wood and bark anatomy of Lauraceae II.
Licaria Aublet. IAWA Bulletin 6:187-199.
Sajeva, M. and J. D. Mauseth. 1991. Leaflike structure in the
Garcia et al.- Anatomy of two species of Echinopsis
photosynthetic, succulent stems of cacti. Annals of Botany
68:405-411.
Silva, J. dos S. V. da, A. Pott, E. L. Cardoso, A. S. de Moraes, S.
M. Salis, V. J. Pott, R. de A. Mauro and S. Galdino. 2000.
Zoneamento ambiental – Borda Oeste do Pantanal: Maciço
do Urucum e Adjacências. Embrapa. 1ª edição. p. 9-22.
Soffiatti, P. and V. Angyalossy. 2003. Stem anatomy of
Cipocereus (Cactaceae). Bradleya 21:39-48.
Soffiatti, P. and V. Angyalossy. 2005. Wood Anatomy of
Cipocereus (Cactaceae). IAWA Journal 26:299-308.
Soffiatti, P. and V. Angyalossy. 2007. Anatomy of Brazilian
Cereeae (subfamily Cactoideae, Cactaceae): Arrojadoa
Britton & Rose, Stephanocereus A. Berger and Brasilicereus
Backeberg. Acta Botanica Brasilica 21:813-822.
Soffiatti, P. and V. Angyalossy. 2009. Increased water storage
capacity in cactus wood: a study in the tribe Cereeae
(Cactoideae, Cactaceae). Haseltonia 15:1-6.
Taylor, N. P. 2000. Cactaceae of estearn Brazil. Ph.D. Thesis,
Royal Botanic Gardens, Kew. p. 414.
Taylor, N. P. and D. C. Zappi. 2004. Cacti of eastern Brazil.
Royal Botanic Gardens, Kew. p. 499.
Terrazas, T. and S. Arias. 2003. Comparative stem anatomy in
the subfamily Cactoideae. The Botanical Review. 68:444-
473.
Terrazas-Salgado, T. and J. D. Mauseth. 2002. Shoot Anatomy
and morphology. In Cacti biology and uses, S. Nobel (ed.).
University of California Press. Berkeley. p. 23-40.